Throughout their lifetime, insects face multiple environmental challenges that influence their performance. Gregarines are prevalent endoparasites in most invertebrates that affect the fitness of their hosts, but are often overlooked in ecological studies. Next to such biotic factors, a current common challenge is anthropogenic pollution with pesticides, which causes a major threat to non-target organisms that are readily exposed to lethal or sublethal concentrations. In a laboratory study, we investigated whether the presence of gregarines modulates the food consumption and life history traits of a (non-target) leaf beetle species, Phaedon cochleariae, in response to sublethal insecticide exposure. We show that the larval food consumption of the herbivore was neither affected by gregarine infection nor sublethal insecticide exposure. Nevertheless, infection with gregarines led to a delayed development, while insecticide exposure resulted in a lower body mass of adult males and a reduced reproduction of females. Individuals exposed to both challenges suffered most, as they had the lowest survival probability. This indicates detrimental effects on the population dynamics of non-target insects infected with naturally occurring gregarines that face additional stress from agrochemical pollution. Moreover, we found that the infection load with gregarines was higher in individuals exposed to sublethal insecticide concentrations compared to unexposed individuals. To counteract the global decline of insects, the potential of natural parasite infections in modulating insect responses to anthropogenic and non-anthropogenic environmental factors should be considered in ecological risk assessment.